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Cecidonius Pampeanus, Gen. Et Sp. N.: an Overlooked and Rare, New Gall-Inducing Micromoth Associated with Schinus in Southern Brazil (Lepidoptera, Cecidosidae)

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Cecidonius Pampeanus, Gen. Et Sp. N.: an Overlooked and Rare, New Gall-Inducing Micromoth Associated with Schinus in Southern Brazil (Lepidoptera, Cecidosidae) A peer-reviewed open-access journal ZooKeys 695: 37–74 (2017) An overlooked and rare new gall-inducing micromoth 37 doi: 10.3897/zookeys.695.13320 RESEARCH ARTICLE http://zookeys.pensoft.net Launched to accelerate biodiversity research Cecidonius pampeanus, gen. et sp. n.: an overlooked and rare, new gall-inducing micromoth associated with Schinus in southern Brazil (Lepidoptera, Cecidosidae) Gilson R.P. Moreira1, Rodrigo P. Eltz1, Ramoim B. Pase1, Gabriela T. Silva2, Sérgio A.L. Bordignon3, Wolfram Mey4, Gislene L. Gonçalves5,6 1 Departamento de Zoologia, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Av. Bento Gonçalves 9500, 91501-970 Porto Alegre, RS, Brazil 2 PPG Biologia Animal, Departamento de Zoologia, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Av. Bento Gonçalves 9500, 91501-970 Porto Alegre, RS, Brazil 3 Programa de Mestrado em Avaliação de Impactos Ambientais, Universidade La Salle, Av. Victor Barreto, 2288, 92010-000 Canoas, RS, Brazil 4 Museum für Naturkunde, Leibniz Institute for Evolution and Biodiversity Science, Invalidenstraße 43, 10115 Berlin, Germany 5 PPG Genética e Biologia Molecular, Departamento de Genética, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Av. Bento Gonçalves 9500, 91501-970 Porto Alegre, RS, Brazil 6 Departamento de Recursos Ambientales, Facultad de Ciencias Agronómicas, Universidad de Tarapacá, Casilla 6-D, Arica, Chile Corresponding author: Gilson R.P. Moreira ([email protected]) Academic editor: E. van Nieukerken | Received 20 April 2017 | Accepted 7 August 2017 | Published 4 September 2017 http://zoobank.org/F9D9BD39-1346-4F18-8EA1-7572C480F300 Citation: Moreira GRP, Eltz RP, Pase RB, Silva GT, Bordignon SAL, Mey W, Gonçalves GL (2017) Cecidonius pampeanus, gen. et sp. n.: an overlooked and rare, new gall-inducing micromoth associated with Schinus in southern Brazil (Lepidoptera: Cecidosidae). ZooKeys 695: 37–74. https://doi.org/10.3897/zookeys.695.13320 Abstract Galls induced by the larval stage of cecidosids (Lepidoptera: Cecidosidae) are complex, multi-trophic systems, still poorly studied. They may be associated with other insect feeding guilds, including inquilines, kleptoparasites, cecidophages, parasitoids, and predators. By causing death of the gall inducer early in life and altering the gall phenotype, inquilines may lead to misidentification of the true gall inducers. Here, we describe through light and scanning electron microscopy Cecidonius pampeanus, a new genus and spe- cies of cecidosid moth, from the Pampa biome, south Brazil. It induces unnoticed, small galls under swol- len stems of Schinus weinmannifolius Mart. ex Engl. (Anacardiaceae). Such galls are severely attacked early in ontogeny either by unidentified parasitoids belonging to Lyrcus Walker (Pteromalidae) that feed upon the inducer, or by inquiline wasps of the genus Allorhogas Gahan (Braconidae). The inquilines modify the galls into large ones that last longer and promptly call attention. Free-living galls are rare and dehiscent, pupation of C. pampeanus occurring on the ground. Due to these reasons the true inducer has been Copyright Gilson R.P. Moreira et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 38 Gilson R.P. Moreira et al. / ZooKeys 695: 37–74 (2017) overlooked in this case for more than a century. Additionally we inferred a phylogeny for Cecidosidae using sequences from mitochondrial and nuclear loci, and characterized genetic variation and gene flow across ten populations. Despite its natural history similarities with the African genus Scyrotis, Cecidonius is a much younger lineage, more closely related to the Neotropical cecidosids. C. pampeanus populations, which are now confined to a few mountain areas within its distribution range due to habitat destruction, are also genetically isolated, requiring conservation measures. Keywords Anacardiaceae, cecidosid moths, conservation, insect galls, Neotropical region, taxonomy Introduction Insect-induced galls may consist of very complex, multitrophic-level systems including not only the gall inducers themselves, but also predators, cecidophages, parasitoids, kleptoparasites and inquilines, among other insects such as successors that use them for shelter. Kleptoparasites in particular invade galls, usurping the cecidogenous spe- cies and become stationary, feeding upon gall tissues until they complete their larval development, and may prey upon the inducer and other insects that eventually enter the usurped gall (e.g., Morris et al. 2000, Luz et al. 2015). They do not induce differen- tiation and growth of new tissues, only feeding on those that were induced to develop by their precursors. Inquilines, however, induce the development of new tissues, either similar to or different from original ones when they take over a given gall, generally killing the inducer by inanition (e.g., Brooks and Shorthouse 1988, van Noort et al. 2007). Thus, they may change substantially the size and shape of the gall they invade. Little attention has been paid to the important taxonomic consequences of this phe- nomenon, a potential difficulty factor in identification of hidden diversity in gall com- munities. Misidentification of the true gall inducers in such cases is obviously likely, since the inducer is eliminated from the system early in the gall ontogeny and no con- spicuous trace of it may be left inside the gall. In addition, contrary to galls attacked either by kleptoparasites or inquilines that may stay attached to host plants, those free of them still containing the growing inducer may be dehiscent, with later develop- ment of immature stages occurring on the ground (e.g., van Noort et al. 2007, Luz et al. 2015). In this case, by altering the place of gall development in the field and thus enhancing the encounter of attacked galls by kleptoparasites and inquilines that stay attached to the host plant compared to free, detached ones, the possibility of missing the presence of the true inducers is substantially increased. Furthermore, depending on the rate of attack by other parasitoids and predators in association, natural densities of the true gall inducer would be reduced further, even becoming rare, and thus may be unnoticed. As a case study, here we describe one example of such a peculiar system, where the induction of a non-conspicuous, dehiscent gall by a cecidosid moth has been overlooked for more than a century, erroneously believed to be induced by their hymenopteran inquilines who do not originally induce galls but in fact modify them early in development into large and colorful, visually appealing galls. An overlooked and rare new gall-inducing micromoth 39 Cecidosidae are poorly known monotrysian Heteroneura moths (sensu Davis 1998), comprising six genera and 18 species, all with ranges restricted to the southern hemi- sphere. They are among a few lepidopteran lineages with a Gondwanic distribution: one occurs in New Zealand, the monotypic genus Xanadoses Hoare & Dugdale; twelve in southern Africa, all belonging to Scyrotis Meyrick, and five in South America, two in Di- cranoses Kieffer & Jörgensen, and three in the monotypic genera Cecidoses Curtis, Euce- cidoses Brèthes, and Oliera Brèthes. Xanadoses nielseni Hoare & Dugdale is a bark-miner of several New Zealand bark trees, particularly within Weinmannia Linnaeus (Cuno- niaceae). Larvae of African Scyrotis form galls on species of Searsia F.A. Barkley (Anac- ardiaceae) (van Noort et al. 2007). In this case, they may also be located in the leaves; these galls are known as “jumping-beans”. They exfoliate from the hostplant and drop to the ground, where they are propelled for short distances by the active pupa inside, a supposed adaptation to avoid excessive heat from the sun (Meyrick 1917, Davis 1998). Unfortunately, none of the immature stages of Scyrotis species have been described in detail yet. South American cecidosids induce galls either on the stem or on axillary buds of Schinus Linnaeus (Anacardiaceae), particularly S. polygamus (Cav.) Cabrera (sensu Ca- brera 1938, Fleig 1987, 1989). Gall morphology and life history of C. eremita Curtis have been treated in detail by Wille (1926). The taxonomy was reviewed and immature stages and galls of O. argentinana Brèthès, and D. capsulifex Kieffer & Jörgensen were described respectively by Moreira et al. (2012) and San Blas and Davis (2013). Informa- tion gathered recently by the first author suggested that diversity of cecidosids is much greater in the Neotropics, and not only additional species of Schinus are used as host but also other Anacardiaceae, such as species of Lithraea Miers ex Hook. & Arn. This study concerns the galls of Schinus weinmannifolius Mart. ex Engl., which are induced by an undescribed genus and species of Cecidosidae in southern Brazil. Although not fully explored yet, the existence of these galls has been known for a long time; their induction was wrongly associated with cynipid wasps (Tavares 1909, Wille 1926, Houard 1933, Sáiz and Núnez 1997). Here the gall, the immature stages, and adults of the true inducer are described under both light and scanning electron micros- copy and provided information on its natural history, in conjunction with a parasitoid and an inquiline wasp frequently found in association with these galls. By conduct-
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